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Loci Impacting Polymorphic Gait in the Tennessee Walking Horse1

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Loci Impacting Polymorphic Gait in the Tennessee Walking Horse1 Loci impacting polymorphic gait in the Tennessee Walking Horse1 E. A. Staiger,* M. A. Abri,† C. A. S. Silva,‡ and S. A. Brooks§2 *Department of Animal Science, Cornell University, Ithaca, NY 14853; †Department of Animal and Veterinary Sciences, College of Agriculture and Marine Sciences, Sultan Qaboos University, PO box 34 Al Khod, Postal Code 123, Muscat, Oman; ‡Department of Animal Science, Instituto Federal Sul-Rio-Grandense, Pelotas, Rio Grande do Sul 96060-290, Brazil; and §Department of Animal Science, University of Florida, Gainesville 32611 Downloaded from https://academic.oup.com/jas/article/94/4/1377/4703958 by guest on 29 September 2021 ABSTRACT: Following domestication, man select- 129 TWH and genotyping was performed at approxi- ed the horse primarily for the purpose of transporta- mately 60,000 loci using the Illumina Equine SNP70 tion rather than consumption; this selective strategy beadchip at GeneSeek Inc. (Lincoln, NE). Case–con- created divergent traits for locomotion. At intermedi- trol association tests identified suggestive regions for ate speeds, beyond the flat walk, the horse can per- gait type on equine chromosome (ECA) 19 (P-value form a range of diagonal and lateral 2-beat or 4-beat of 1.50 × 10–5 after 1 million permutations; PLINK gait patterns. The Tennessee Walking Horse (TWH) version 1.07). Haplotype analysis identified 2 sig- is the only U.S. breed able to perform an even-timed nificant haplotypes on ECA19 and ECA11 (P-values 4-beat gait (the “running-walk”) at intermediate of 3.7 × 10–5 and 3.92 × 10–5, respectively). Genes speeds; however, within the breed, there is remaining within these suggestive regions play roles in develop- variation in gait type. To investigate the contribution mental processes and biological regulation, indicat- of genetics to this unique trait, blood or hair samples ing there may be variant differences in the neurobiol- for DNA and gait information were collected from ogy and regulation of horses with a polymorphic gait. Key words: gait, genome-wide association study, horse, running walk © 2016 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2016.94:1377–1386 doi:10.2527/jas2015-9936 INTRODUCTION out a moment of suspension is commonly called a “gaited” horse. The horse is a unique model for the Horses are polymorphic in the pattern and tim- study of gait development, as no other mammalian ing of locomotion. At intermediate speeds, the horse species is known to discretely segregate for con- can perform a range of diagonal and lateral 2-beat or genital differences in stride cadence and footfall pat- 4-beat footfall patterns (Harris, 1993). A horse with tern. Laboratory-induced models of variation in gait the ability to perform any of the 4-beat gaits with- exist in mice and cats via transverse sectioning of the spinal cord (Grillner and Zangger, 1979) and in- 1This work was supported in part by a seed grant from the duced mutations or knockouts in mice (Coonan et al., Cornell Center for Vertebrate Genomics, by the USDA National 2001; Kullander et al., 2001; Hinckley et al., 2005; Institute of Food and Agriculture, Hatch project NYC-127454, and Wilson et al., 2005; Crone et al., 2008). These labo- by a grant from the Foundation for the Advancement and Support ratory models enabled discovery of localized neural of the Tennessee Walking Show Horse. Any opinions, findings, networks known as central pattern generators (CPG; conclusions, or recommendations expressed in this publication are Kuo, 2002). When locomotion is initiated, activity those of the authors and do not necessarily reflect the view of the in the CPG is turned on and maintained by inputs National Institute of Food and Agriculture (NIFA) or the United from descending locomotor commands originating States Department of Agriculture (USDA). We appreciate the help from neurons in the brainstem and midbrain (Kiehn, of all contributing owners, breeders, and trainers. 2006). Naturally occurring models of lateral gait, 2Corresponding author: [email protected] Received October 2, 2015. such as horses, provide a novel resource for study of Accepted January 29, 2016. CPG structure and function. 1377 1378 Staiger et al. Downloaded from https://academic.oup.com/jas/article/94/4/1377/4703958 by guest on 29 September 2021 Figure 1. Two foals that exemplify variation in gait types in Tennessee Walking horses. (A) The diagonal trot of a multigaited horse (foal is 2 mo old) and (B) the lateral amble of a lateral-only horse (foal is 2 d old). The Tennessee Walking Horse (TWH) is a U.S. travel, approximately at the horse’s wither height, and breed renowned for their ability to perform an even- far enough away that the horse fit within the camera’s timed 4-beat gait (the “running-walk”) at intermedi- view finder. We recorded each horse for at least 10 s at ate speeds. The TWH is nearly fixed for the DMRT3 the walk and all intermediate gaits. We also collected mutation (Promerová et al., 2014). However, TWH level of training under saddle, horse discipline (breed- are capable of performing the whole range of inter- ing, trail, and show), type of shoes (barefoot, alumi- mediate gaits from 2-beat lateral to 4-beat to 2-beat num, steel, and pad), and pedigree information. diagonal (Tennessee Walking Horse Breeders’ and A single experienced observer classified horses Exhibitors’ Association, 2011). At liberty, these horses as either lateral only or multigaited (able to perform show an innate preference for either trot, pace, or run- both lateral and diagonal gaits, including the trot) after ning walk from birth (Fig. 1). The objective of this review of video recordings in slow motion. The in- study is to identify candidate loci and SNPs unique to dividual classified horses as lateral-only gaited if the gait type variation within the TWH breed through a lateral pair of legs traveled together in a 4-beat pat- genome-wide association study (GWAS). tern (with the hind hoof landing before the front hoof). If the footfall landing followed a 2-beat or 4-beat di- MATERIALS AND METHODS agonal pattern and the lateral gait pattern previously described was also observed, the individual classified All animal procedures were approved by the the horse as multigaited. Horses were also classified Cornell University Institutional Animal Care and Use as multigaited if the owner reported viewing the horse Committee (protocol 2008-0121). trotting at liberty but not in the video analysis (n = 9). Eighty-two horses were classified as lateral only and Animals and Phenotypes 57 as multigaited in a case–control GWAS design. Pedigree information, as contained in the reg- We collected 139 TWH samples from 55 private istry or reported by the owner, was recorded for 137 farms and public horse shows across the United States horses; the remaining 2 horses were registered, but the during a period from 2010 to 2015 for use in this study. registration papers including the pedigree had been The group consisted of 82 mares and 57 geldings and lost. Horses were selected so that no horse was a first- stallions ranging from 1 to 34 yr in age at time of col- generation relative to any other within a given phe- lection. We video recorded all horses either under sad- notypic category to reduce population stratification. dle, at liberty in a round pen, or in hand at the walk and Half-siblings (n = 17 pairs) or parent–offspring pairs at all intermediate gaits using a Canon FS30 camcord- (n = 8 pairs) were only used if 1 member of each pair er (Canon Inc., Tokyo, Japan). The camcorder was set had been classified as lateral-only gaited and the other up so that it was perpendicular to the horse’s plane of as multigaited to balance any stratification across the Genetics of gait in Tennessee Walking horses 1379 2 gait phenotypes. Pedigraph version 2.4 (Garbe and TWH randomly selected from this study to analyze Da, 2008) and the 5-generation pedigrees were used population structure. Values were binned in groups to evaluate the inbreeding within the 137 horses. In of 5,000 consecutive markers, and average r2 and the 2 cases where pedigree information was not avail- inter-SNP distance were graphed using Excel 2007 able, we calculated genome-sharing ( pi ) values and (Microsoft Corp., New York, NY). inbreeding (F) for the autosomes across all 139 indi- viduals in PLINK (Purcell et al., 2007) after pruning DMRT3 Amplification and Genotyping for minor allele frequency (MAF) of 0.05 and geno- typing rate of 0.05. A recent publication describes a mutation in the DMRT3 gene, which is suggested to control for the Deoxyribonucleic Acid Extraction, Genotyping, ability for a horse to perform lateral patterned gaits and Quality Control (Andersson et al., 2012). We examined the effect of this mutation in our study population, following a Downloaded from https://academic.oup.com/jas/article/94/4/1377/4703958 by guest on 29 September 2021 We isolated genomic DNA from blood samples using previously published protocol developed in our lab the Gentra Puregene Blood Kit, following the manufac- (Patterson et al., 2015). turer’s protocol for whole blood (Qiagen Inc., Valencia, CA). We performed extraction of DNA from hair using Statistical Analysis the Gentra Puregene DNA Isolation Kit, following the manufacturer’s protocol with modifications to optimize PLINK version 1.07 (Purcell et al., 2007) and SVS for hair root bulbs (Qiagen Inc.; Cook et al., 2010). software from Golden Helix, Inc. (http://goldenhelix. We genotyped 139 TWH with complete gait phe- com; accessed December 5, 2014) were both used to notypes at 65,157 loci using the Equine SNP70K bead- test the resulting 42,226 genotypes in 129 individuals chip (Illumina Inc., San Diego, CA) at GeneSeek Inc.
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